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      Shared facial emotion processing functional network findings in medication-naïve major depressive disorder and healthy individuals: detection by sICA

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          Abstract

          Background

          The fundamental mechanism underlying emotional processing in major depressive disorder (MDD) remains unclear. To better understand the neural correlates of emotional processing in MDD, we investigated the role of multiple functional networks (FNs) during emotional stimuli processing.

          Methods

          Thirty-two medication-naïve subjects with MDD and 36 healthy controls (HCs) underwent an emotional faces fMRI task that included neutral, happy and fearful expressions. Spatial independent component analysis (sICA) and general linear model (GLM) were conducted to examine the main effect of task condition and group, and two-way interactions of group and task conditions.

          Results

          In sICA analysis, MDD patients and HCs together showed significant differences in task-related modulations in five FNs across task conditions. One FN mainly involving the ventral medial prefrontal cortex showed lower activation during fearful relative to happy condition. Two FNs mainly involving the bilateral inferior frontal gyrus and temporal cortex, showed opposing modulation relative to the ventral medial prefrontal cortex FN, i.e., greater activation during fearful relative to happy condition. Two remaining FNs involving the fronto-parietal and occipital cortices, showed reduced activation during both fearful and happy conditions relative to the neutral condition. However, MDD and HCs did not show significant differences in expression-related modulations in any FNs in this sample.

          Conclusions

          SICA revealed differing functional activation patterns than typical GLM-based analyses. The sICA findings demonstrated unique FNs involved in processing happy and fearful facial expressions. Potential differences between MDD and HCs in expression-related FN modulation should be investigated further.

          Electronic supplementary material

          The online version of this article (10.1186/s12888-018-1631-0) contains supplementary material, which is available to authorized users.

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          Most cited references62

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          Evidence for a frontoparietal control system revealed by intrinsic functional connectivity.

          Two functionally distinct, and potentially competing, brain networks have been recently identified that can be broadly distinguished by their contrasting roles in attention to the external world versus internally directed mentation involving long-term memory. At the core of these two networks are the dorsal attention system and the hippocampal-cortical memory system, a component of the brain's default network. Here spontaneous blood-oxygenation-level-dependent (BOLD) signal correlations were used in three separate functional magnetic resonance imaging data sets (n = 105) to define a third system, the frontoparietal control system, which is spatially interposed between these two previously defined systems. The frontoparietal control system includes many regions identified as supporting cognitive control and decision-making processes including lateral prefrontal cortex, anterior cingulate cortex, and inferior parietal lobule. Detailed analysis of frontal and parietal cortex, including use of high-resolution data, revealed clear evidence for contiguous but distinct regions: in general, the regions associated with the frontoparietal control system are situated between components of the dorsal attention and hippocampal-cortical memory systems. The frontoparietal control system is therefore anatomically positioned to integrate information from these two opposing brain systems.
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            Neurons in medial prefrontal cortex signal memory for fear extinction.

            Conditioned fear responses to a tone previously paired with a shock diminish if the tone is repeatedly presented without the shock, a process known as extinction. Since Pavlov it has been hypothesized that extinction does not erase conditioning, but forms a new memory. Destruction of the ventral medial prefrontal cortex, which consists of infralimbic and prelimbic cortices, blocks recall of fear extinction, indicating that medial prefrontal cortex might store long-term extinction memory. Here we show that infralimbic neurons recorded during fear conditioning and extinction fire to the tone only when rats are recalling extinction on the following day. Rats that froze the least showed the greatest increase in infralimbic tone responses. We also show that conditioned tones paired with brief electrical stimulation of infralimbic cortex elicit low freezing in rats that had not been extinguished. Thus, stimulation resembling extinction-induced infralimbic tone responses is able to simulate extinction memory. We suggest that consolidation of extinction learning potentiates infralimbic activity, which inhibits fear during subsequent encounters with fear stimuli.
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              Neurobiology of emotion perception II: Implications for major psychiatric disorders.

              To date, there has been little investigation of the neurobiological basis of emotion processing abnormalities in psychiatric populations. We have previously discussed two neural systems: 1) a ventral system, including the amygdala, insula, ventral striatum, ventral anterior cingulate gyrus, and prefrontal cortex, for identification of the emotional significance of a stimulus, production of affective states, and automatic regulation of emotional responses; and 2) a dorsal system, including the hippocampus, dorsal anterior cingulate gyrus, and prefrontal cortex, for the effortful regulation of affective states and subsequent behavior. In this critical review, we have examined evidence from studies employing a variety of techniques for distinct patterns of structural and functional abnormalities in these neural systems in schizophrenia, bipolar disorder, and major depressive disorder. In each psychiatric disorder, the pattern of abnormalities may be associated with specific symptoms, including emotional flattening, anhedonia, and persecutory delusions in schizophrenia, prominent mood swings, emotional lability, and distractibility in bipolar disorder during depression and mania, and with depressed mood and anhedonia in major depressive disorder. We suggest that distinct patterns of structural and functional abnormalities in neural systems important for emotion processing are associated with specific symptoms of schizophrenia and bipolar and major depressive disorder.
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                Author and article information

                Contributors
                xikuang512@163.com
                edmistonk@upmc.edu
                yanqingtang@163.com
                fanguog@vip.sina.com
                kexu@vip.sina.com , kexu@vip.sina.com
                fei.wang@mail.cmu.edu.cn
                Journal
                BMC Psychiatry
                BMC Psychiatry
                BMC Psychiatry
                BioMed Central (London )
                1471-244X
                10 April 2018
                10 April 2018
                2018
                : 18
                : 96
                Affiliations
                [1 ]GRID grid.412636.4, Department of Radiology, , The First Hospital of China Medical University, ; Shenyang, Liaoning People’s Republic of China
                [2 ]ISNI 0000 0004 1936 9000, GRID grid.21925.3d, Department of Psychiatry, , University of Pittsburgh School of Medicine, ; Pittsburgh, PA USA
                [3 ]GRID grid.412636.4, Department of Psychiatry, , The First Hospital of China Medical University, ; Shenyang, Liaoning People’s Republic of China
                [4 ]ISNI 0000000419368710, GRID grid.47100.32, Department of Psychiatry, , Yale University School of Medicine, ; New Haven, CT USA
                Article
                1631
                10.1186/s12888-018-1631-0
                5891939
                29636031
                26533e2e-90c6-4471-b197-f91d939e457b
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 29 November 2016
                : 9 February 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 81571311
                Award ID: 81071099
                Award ID: 81271499
                Award ID: 81571331
                Award Recipient :
                Funded by: National Institution of Health
                Award ID: K01MH086621
                Funded by: Liaoning Pandeng Scholar
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Clinical Psychology & Psychiatry
                Clinical Psychology & Psychiatry

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